Transcriptomic and morphophysiological evidence for a specialized human cortical GABAergic cell type

We describe convergent evidence from transcriptomics, morphology, and physiology for a specialized GABAergic neuron subtype in human cortex. Using unbiased single-nucleus RNA sequencing, we identify ten GABAergic interneuron subtypes with combinatorial gene signatures in human cortical layer 1 and c...

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Published inNature neuroscience Vol. 21; no. 9; pp. 1185 - 1195
Main Authors Boldog, Eszter, Bakken, Trygve E., Hodge, Rebecca D., Novotny, Mark, Aevermann, Brian D., Baka, Judith, Bordé, Sándor, Close, Jennie L., Diez-Fuertes, Francisco, Ding, Song-Lin, Faragó, Nóra, Kocsis, Ágnes K., Kovács, Balázs, Maltzer, Zoe, McCorrison, Jamison M., Miller, Jeremy A., Molnár, Gábor, Oláh, Gáspár, Ozsvár, Attila, Rózsa, Márton, Shehata, Soraya I., Smith, Kimberly A., Sunkin, Susan M., Tran, Danny N., Venepally, Pratap, Wall, Abby, Puskás, László G., Barzó, Pál, Steemers, Frank J., Schork, Nicholas J., Scheuermann, Richard H., Lasken, Roger S., Lein, Ed S., Tamás, Gábor
Format Journal Article
LanguageEnglish
Published New York Nature Publishing Group US 01.09.2018
Nature Publishing Group
Subjects
631/378/3920
631/378/87
9/74
Adult
Aged
Animal Genetics and Genomics
Axons - ultrastructure
Behavioral Sciences
Biological Techniques
Biomedical and Life Sciences
Biomedicine
Brain
Brain research
Cells (Biology)
Cerebral Cortex - metabolism
Cerebral Cortex - ultrastructure
Cholecystokinin
Combinatorial analysis
Cortex
Cytology
Dendritic Spines - metabolism
Dendritic Spines - ultrastructure
Dendritic structure
Excavation
GABA
GABAergic Neurons - metabolism
GABAergic Neurons - ultrastructure
Gap junctions
Gap Junctions - metabolism
Gap Junctions - ultrastructure
Gene expression
Gene Library
Gene sequencing
Genes
Genomics
Glutamate decarboxylase
Humans
Information processing
Interneurons
Male
Morphology
Neural circuitry
Neurobiology
Neurons
Neurosciences
Observations
Physiology
Polymerase Chain Reaction
Presynapse
Presynaptic Terminals - metabolism
Presynaptic Terminals - ultrastructure
Properties
Pyramidal cells
Pyramidal Cells - metabolism
Pyramidal Cells - ultrastructure
Quality control
Ribonucleic acid
RNA
RNA - analysis
RNA - genetics
RNA sequencing
Rodents
Sequence Analysis, RNA
Transcriptome
γ-Aminobutyric acid
Online AccessGet full text

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Abstract We describe convergent evidence from transcriptomics, morphology, and physiology for a specialized GABAergic neuron subtype in human cortex. Using unbiased single-nucleus RNA sequencing, we identify ten GABAergic interneuron subtypes with combinatorial gene signatures in human cortical layer 1 and characterize a group of human interneurons with anatomical features never described in rodents, having large ‘rosehip’-like axonal boutons and compact arborization. These rosehip cells show an immunohistochemical profile (GAD1 + CCK + , CNR1 – SST – CALB2 – PVALB – ) matching a single transcriptomically defined cell type whose specific molecular marker signature is not seen in mouse cortex. Rosehip cells in layer 1 make homotypic gap junctions, predominantly target apical dendritic shafts of layer 3 pyramidal neurons, and inhibit backpropagating pyramidal action potentials in microdomains of the dendritic tuft. These cells are therefore positioned for potent local control of distal dendritic computation in cortical pyramidal neurons. The authors use single-nucleus RNA-seq to identify 10 GABAergic interneuron subtypes in human cortex layer 1. Molecular, morphological, and physiological evidence points to an emerging human cell type, the rosehip cell, not found in other species.
AbstractList We describe convergent evidence from transcriptomics, morphology and physiology for a specialized GABAergic neuron subtype in human cortex. Using unbiased single nucleus RNA sequencing, we identify ten GABAergic interneuron subtypes with combinatorial gene signatures in human cortical layer 1 and characterize a novel group of human interneurons with anatomical features never described in rodents having large, “rosehip”-like axonal boutons and compact arborization. These rosehip cells show an immunohistochemical profile (GAD1/CCK-positive, CNR1/SST/CALB2/PVALB-negative) matching a single transcriptomically-defined cell type whose specific molecular marker signature is not seen in mouse cortex. Rosehip cells in layer 1 make homotypic gap junctions, predominantly target apical dendritic shafts of layer 3 pyramidal neurons and inhibit backpropagating pyramidal action potentials in microdomains of the dendritic tuft. These cells are therefore positioned for potent local control of distal dendritic computation in cortical pyramidal neurons.
We describe convergent evidence from transcriptomics, morphology, and physiology for a specialized GABAergic neuron subtype in human cortex. Using unbiased single-nucleus RNA sequencing, we identify ten GABAergic interneuron subtypes with combinatorial gene signatures in human cortical layer 1 and characterize a group of human interneurons with anatomical features never described in rodents, having large 'rosehip'-like axonal boutons and compact arborization. These rosehip cells show an immunohistochemical profile (GAD1.sup.+CCK.sup.+, CNR1.sup.-SST.sup.-CALB2.sup.-PVALB.sup.-) matching a single transcriptomically defined cell type whose specific molecular marker signature is not seen in mouse cortex. Rosehip cells in layer 1 make homotypic gap junctions, predominantly target apical dendritic shafts of layer 3 pyramidal neurons, and inhibit backpropagating pyramidal action potentials in microdomains of the dendritic tuft. These cells are therefore positioned for potent local control of distal dendritic computation in cortical pyramidal neurons. The authors use single-nucleus RNA-seq to identify 10 GABAergic interneuron subtypes in human cortex layer 1. Molecular, morphological, and physiological evidence points to an emerging human cell type, the rosehip cell, not found in other species.
We describe convergent evidence from transcriptomics, morphology, and physiology for a specialized GABAergic neuron subtype in human cortex. Using unbiased single-nucleus RNA sequencing, we identify ten GABAergic interneuron subtypes with combinatorial gene signatures in human cortical layer 1 and characterize a group of human interneurons with anatomical features never described in rodents, having large 'rosehip'-like axonal boutons and compact arborization. These rosehip cells show an immunohistochemical profile (GAD1.sup.+CCK.sup.+, CNR1.sup.-SST.sup.-CALB2.sup.-PVALB.sup.-) matching a single transcriptomically defined cell type whose specific molecular marker signature is not seen in mouse cortex. Rosehip cells in layer 1 make homotypic gap junctions, predominantly target apical dendritic shafts of layer 3 pyramidal neurons, and inhibit backpropagating pyramidal action potentials in microdomains of the dendritic tuft. These cells are therefore positioned for potent local control of distal dendritic computation in cortical pyramidal neurons.
We describe convergent evidence from transcriptomics, morphology, and physiology for a specialized GABAergic neuron subtype in human cortex. Using unbiased single-nucleus RNA sequencing, we identify ten GABAergic interneuron subtypes with combinatorial gene signatures in human cortical layer 1 and characterize a group of human interneurons with anatomical features never described in rodents, having large ‘rosehip’-like axonal boutons and compact arborization. These rosehip cells show an immunohistochemical profile (GAD1+CCK+, CNR1–SST–CALB2–PVALB–) matching a single transcriptomically defined cell type whose specific molecular marker signature is not seen in mouse cortex. Rosehip cells in layer 1 make homotypic gap junctions, predominantly target apical dendritic shafts of layer 3 pyramidal neurons, and inhibit backpropagating pyramidal action potentials in microdomains of the dendritic tuft. These cells are therefore positioned for potent local control of distal dendritic computation in cortical pyramidal neurons.
We describe convergent evidence from transcriptomics, morphology, and physiology for a specialized GABAergic neuron subtype in human cortex. Using unbiased single-nucleus RNA sequencing, we identify ten GABAergic interneuron subtypes with combinatorial gene signatures in human cortical layer 1 and characterize a group of human interneurons with anatomical features never described in rodents, having large 'rosehip'-like axonal boutons and compact arborization. These rosehip cells show an immunohistochemical profile (GAD1 CCK , CNR1 SST CALB2 PVALB ) matching a single transcriptomically defined cell type whose specific molecular marker signature is not seen in mouse cortex. Rosehip cells in layer 1 make homotypic gap junctions, predominantly target apical dendritic shafts of layer 3 pyramidal neurons, and inhibit backpropagating pyramidal action potentials in microdomains of the dendritic tuft. These cells are therefore positioned for potent local control of distal dendritic computation in cortical pyramidal neurons.
We describe convergent evidence from transcriptomics, morphology, and physiology for a specialized GABAergic neuron subtype in human cortex. Using unbiased single-nucleus RNA sequencing, we identify ten GABAergic interneuron subtypes with combinatorial gene signatures in human cortical layer 1 and characterize a group of human interneurons with anatomical features never described in rodents, having large 'rosehip'-like axonal boutons and compact arborization. These rosehip cells show an immunohistochemical profile (GAD1+CCK+, CNR1-SST-CALB2-PVALB-) matching a single transcriptomically defined cell type whose specific molecular marker signature is not seen in mouse cortex. Rosehip cells in layer 1 make homotypic gap junctions, predominantly target apical dendritic shafts of layer 3 pyramidal neurons, and inhibit backpropagating pyramidal action potentials in microdomains of the dendritic tuft. These cells are therefore positioned for potent local control of distal dendritic computation in cortical pyramidal neurons.We describe convergent evidence from transcriptomics, morphology, and physiology for a specialized GABAergic neuron subtype in human cortex. Using unbiased single-nucleus RNA sequencing, we identify ten GABAergic interneuron subtypes with combinatorial gene signatures in human cortical layer 1 and characterize a group of human interneurons with anatomical features never described in rodents, having large 'rosehip'-like axonal boutons and compact arborization. These rosehip cells show an immunohistochemical profile (GAD1+CCK+, CNR1-SST-CALB2-PVALB-) matching a single transcriptomically defined cell type whose specific molecular marker signature is not seen in mouse cortex. Rosehip cells in layer 1 make homotypic gap junctions, predominantly target apical dendritic shafts of layer 3 pyramidal neurons, and inhibit backpropagating pyramidal action potentials in microdomains of the dendritic tuft. These cells are therefore positioned for potent local control of distal dendritic computation in cortical pyramidal neurons.
We describe convergent evidence from transcriptomics, morphology, and physiology for a specialized GABAergic neuron subtype in human cortex. Using unbiased single-nucleus RNA sequencing, we identify ten GABAergic interneuron subtypes with combinatorial gene signatures in human cortical layer 1 and characterize a group of human interneurons with anatomical features never described in rodents, having large ‘rosehip’-like axonal boutons and compact arborization. These rosehip cells show an immunohistochemical profile (GAD1 + CCK + , CNR1 – SST – CALB2 – PVALB – ) matching a single transcriptomically defined cell type whose specific molecular marker signature is not seen in mouse cortex. Rosehip cells in layer 1 make homotypic gap junctions, predominantly target apical dendritic shafts of layer 3 pyramidal neurons, and inhibit backpropagating pyramidal action potentials in microdomains of the dendritic tuft. These cells are therefore positioned for potent local control of distal dendritic computation in cortical pyramidal neurons. The authors use single-nucleus RNA-seq to identify 10 GABAergic interneuron subtypes in human cortex layer 1. Molecular, morphological, and physiological evidence points to an emerging human cell type, the rosehip cell, not found in other species.
Audience Academic
Author Novotny, Mark
Faragó, Nóra
Oláh, Gáspár
Schork, Nicholas J.
Boldog, Eszter
Hodge, Rebecca D.
Maltzer, Zoe
Wall, Abby
Ozsvár, Attila
Aevermann, Brian D.
Shehata, Soraya I.
Venepally, Pratap
Close, Jennie L.
Diez-Fuertes, Francisco
Ding, Song-Lin
Lein, Ed S.
Kovács, Balázs
Barzó, Pál
Molnár, Gábor
Tran, Danny N.
Tamás, Gábor
Steemers, Frank J.
Sunkin, Susan M.
Rózsa, Márton
Bakken, Trygve E.
Scheuermann, Richard H.
Puskás, László G.
McCorrison, Jamison M.
Bordé, Sándor
Lasken, Roger S.
Smith, Kimberly A.
Baka, Judith
Kocsis, Ágnes K.
Miller, Jeremy A.
AuthorAffiliation 1 MTA-SZTE Research Group for Cortical Microcircuits, Department of Anatomy, Physiology and Neuroscience, University of Szeged, Közép fasor 52., Szeged, H-6726, Hungary
4 Illumina, Inc., 5200 Illumina Way, San Diego, CA 92122 USA
7 Department of Pathology, 9500 Gilman Drive, University of California, San Diego, CA 92093 USA
2 Allen Institute for Brain Science, 615 Westlake Avenue North, Seattle, WA 98109, USA
3 J. Craig Venter Institute, 4120 Capricorn Lane, La Jolla, CA 92037, USA
6 Department of Neurosurgery, University of Szeged, Hungary, Semmelweis u. 6., Szeged, H-6725 Hungary
5 Laboratory of Functional Genomics, Department of Genetics, Biological Research Center, Hungarian Academy of Sciences, Temesvári krt. 62, H-6726, Szeged, Hungary
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/30150662$$D View this record in MEDLINE/PubMed
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Snippet We describe convergent evidence from transcriptomics, morphology, and physiology for a specialized GABAergic neuron subtype in human cortex. Using unbiased...
We describe convergent evidence from transcriptomics, morphology and physiology for a specialized GABAergic neuron subtype in human cortex. Using unbiased...
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SubjectTerms 631/378/3920
631/378/87
9/74
Adult
Aged
Animal Genetics and Genomics
Axons - ultrastructure
Behavioral Sciences
Biological Techniques
Biomedical and Life Sciences
Biomedicine
Brain
Brain research
Cells (Biology)
Cerebral Cortex - metabolism
Cerebral Cortex - ultrastructure
Cholecystokinin
Combinatorial analysis
Cortex
Cytology
Dendritic Spines - metabolism
Dendritic Spines - ultrastructure
Dendritic structure
Excavation
GABA
GABAergic Neurons - metabolism
GABAergic Neurons - ultrastructure
Gap junctions
Gap Junctions - metabolism
Gap Junctions - ultrastructure
Gene expression
Gene Library
Gene sequencing
Genes
Genomics
Glutamate decarboxylase
Humans
Information processing
Interneurons
Male
Morphology
Neural circuitry
Neurobiology
Neurons
Neurosciences
Observations
Physiology
Polymerase Chain Reaction
Presynapse
Presynaptic Terminals - metabolism
Presynaptic Terminals - ultrastructure
Properties
Pyramidal cells
Pyramidal Cells - metabolism
Pyramidal Cells - ultrastructure
Quality control
Ribonucleic acid
RNA
RNA - analysis
RNA - genetics
RNA sequencing
Rodents
Sequence Analysis, RNA
Transcriptome
γ-Aminobutyric acid
Title Transcriptomic and morphophysiological evidence for a specialized human cortical GABAergic cell type
URI https://link.springer.com/article/10.1038/s41593-018-0205-2
https://www.ncbi.nlm.nih.gov/pubmed/30150662
https://www.proquest.com/docview/2097574601
https://www.proquest.com/docview/2095528620
https://pubmed.ncbi.nlm.nih.gov/PMC6130849
Volume 21
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